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Patterns of Chasmogamy and Cleistogamy, a Mixed-Mating Strategy in an Endangered Perennial

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Patterns of Chasmogamy and Cleistogamy, a Mixed-Mating Strategy in an Endangered Perennial Research Article Patterns of chasmogamy and cleistogamy, a mixed-mating strategy in an endangered perennial Stephanie M. Koontz1*, Carl W. Weekley1, Sarah J. Haller Crate2 and Eric S. Menges1 1The Plant Ecology Program, Archbold Biological Station, Lake Placid, FL 33862, USA 2Longleaf Program Coordinator, North Carolina Forest Service, North Carolina Department of Agriculture and Consumer Services, Raleigh, NC 27699, USA Received: 16 December 2016 Editorial decision: 14 October 2017 Accepted: 30 October 2017 Published: 7 November 2017 Associate Editor: Joseph H. Williams, Jr. Citation: Koontz SM, Weekley CW, Haller Crate SJ, Menges ES. 2017. Experimental evidence for benefit of self discrimination in roots of a clonal plant. AoB PLANTS 9: plx059; doi: 10.1093/aobpla/plx059 Abstract. Cleistogamy (CL) in angiosperms historically has been understudied; however, its co-occurrence with chasmogamy (CH) across many plant species suggests a fitness advantage to maintaining this mixed-mating strategy. Maintenance of mixed-mating has been attributed to reproductive assurance, resource allocation or gen- etic trade-offs. Our goals were to explore patterns of CH and CL, quantify reproductive contributions measured by fruit production and determine how CL is maintained in the endangered perennial Polygala lewtonii. This species exhibits CH and both above-ground cleistogamy (CL-AG) and below-ground cleistogamy (CL-BG). In monthly cen- suses from 2008 to 2012, we documented flowering patterns by counting CH flowering stems, CL-AG fruits and CL-BG rhizomes per plant. Monitoring of buds on CH flowering stems in 2004 provided an estimate of CH fruits per plant. Plant excavations in 2005 of CL-BG rhizomes provided an estimate of CL-BG fruits per plant. Floral morphs were temporally separated with CH flowers observed from January to May and CL flowers from June to February. Overall, 17.5 % of plants flowered; most plants expressed CH first in spring months (63.4 %) and the rest initiated CL-AG in fall months. Reproductive output was dominated by CH (median 26 fruits) compared to combined CL (me- dian 3.5 fruits). Annual reproductive effort of CL-AG was positively correlated with plant age while CH had no rela- tion. Our research shows CH as the dominant form of reproductive effort with most individuals expressing CH and through greater reproductive contributions. CL appears limited by plant size or resources based on the positive relationship with plant age. CL dependency on resource availability is common in other species found in dry or low- quality habitats; however, CL contributions in this species are comparatively low. This raises more questions related to energy requirements of both floral morphs, how this affects the production of viable progeny and why CL persists. Keywords: Amphicarpy; chasmogamy; cleistogamy; flower dimorphism; resource availability; spatial and temporal variation. Introduction progeny while preserving locally adapted alleles. This mixed-mating was once thought to be evolutionar- Mixed-mating in plants can provide a unique fitness ily unstable; however, multiple reproductive strategies advantage through the production of genetically diverse occur frequently in vascular plants, with 42 % of species *Corresponding author’s e-mail address: [email protected] © The Author(s) 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. AoB PLANTS https://academic.oup.com/aobpla © The Authors 2017 1 Downloaded from https://academic.oup.com/aobpla/article-abstract/9/6/plx059/4600026 by guest on 15 February 2018 Koontz et al. – Patterns of chasmogamy and cleistogamy in Polygala lewtonii examined exhibiting some form of mixed reproduction more effective at purging deleterious alleles (Lande and (Goodwille et al. 2005). In a separate review, cleistogamy Schmske 1985; Charlesworth and Charlesworth 1987) (CL; closed, self-pollinating flowers) was documented in while genetically more diverse outcrossed progeny are 693 species across 50 families and 77 % of these also maintained through heterosis (Lu 2002; Oakley et al. had chasmogaous, presumably outcrossed flowers 2007). (dimorphic CL; Culley and Klooster 2007). The frequency Here, we document the pattern of mixed-mating in the in which mixed-mating strategies have occurred sug- rare Polygala lewtonii (Polygalaceae), a federally endan- gests there is strong selection pressure for producing gered perennial herb (USFWS 1999; Coile and Garland mixed progeny. 2003) found on only two ancient sand dune ridges Strategies for mixed-mating systems can occur with (Mount Dora and Lake Wales Ridges) in central Florida. the production of open-pollinated chasmogamous Its primary habitat is sandhill, dominated by long- flowers and permanently closed self-pollinating cleis- leaf pine-wiregrass assemblages on xeric yellow sands, togamous flowers (Lord 1981; Schoen and Lloyd 1984; an ecosystem shaped by frequent fire (1–10 years; Myers Culley and Klooster 2007), with both self-compatible 1990; Menges 1999) and seasonal fluctuations in rain- and incompatible individuals (Stone 2002) or with indi- fall (dry winters and wet summers) and temperature vidual flowers forming either outcrossed or selfed fruits (summer temperatures > 30 °C; Menges 1999). Polygala (Schoen and Brown 1991). Chasmogamous flowers, lewtonii adults are killed by fire but seedlings recruit when cross-pollinated, produce genetically diverse pro- post-fire from a persistent soil seed bank (Weekley and geny, thus maintaining genetic diversity, while cleistog- Menges 2012). In the absence of fire, populations de- amous progeny possess only maternal information and cline and may disappear above-ground. preserve locally adapted genes (Schoen and Lloyd 1984; Polygala lewtonii is one of three species within the Waller 1984; Mitchell-Olds and Waller 1985; Schmitt family Polygalaceae exhibiting CL (Lord 1981; Culley et al. 1985; Winn and Moriuchi 2009). Chasmogamy and Klooster 2007). Both P. polygama and P. pauciflora (CH) usually relies on pollinator availability for pollen exhibit amphicarpy and observational studies suggest transfer, although self-pollination is also possible in their mixed-mating systems are maintained through re- some species. Chasmogamous flowers typically are en- source allocation (Shaw 1901). CL in P. lewtonii was first ergetically more expensive to produce and have lower briefly described by James (1957) as the species’ ability seed set compared to cleistogamous flowers (Schemske to set seed in both open and closed flowers. Small dark 1978; Waller 1979; Schoen and Lloyd 1984; Mitchell-Olds purple to pink chasmogamous flowers are clustered on and Waller 1985). CL increases a populations’ suscepti- terminal racemes. Chasmogamous flowers rely on in- bility to genetic drift and inbreeding depression if dele- sect pollinators and delayed selfing is rare (Weekley and terious alleles cannot be purged (Lloyd 1979; Lande and Brothers 2006). Aerial cleistogamous flowers are incon- Schemske 1985). These fitness trade-offs are factors in spicuous, green to pale pink and solitary in the lower leaf maintaining a mixed-mating strategy. axils. Subterranean CL occurs on rhizomes extending There are several hypotheses explaining natural from the base of the plant. A recent study examining the selection leading to the maintenance of mixed-mating spatial genetics of P. lewtonii suggested most recruit- strategies (Goodwillie et al. 2005; Oakley et al. 2007). ment is from cleistogamous seeds (Swift et al. 2016). Reproductive assurance describes selfing as a backup For the remainder of this study we refer to chasmogamy mechanism when pollen is limiting or stochastic events as CH, above-ground cleistogamy as CL-AG and below- occur (Le Corff 1993; Masuda and Yahara 1994; Culley ground cleistogamy as CL-BG. 2002). Here, production of cleistogamous flowers is Understanding reproductive patterns and limita- dependent on the relative success of CH and floral tions of P. lewtonii can provide needed insight to its morphs are separated temporally or spatially to ensure reproductive ecology and better inform conservation progeny success (Berg and Redbo-Torstensson 1998). efforts. The goal of this study was to characterize CH Another hypothesis is that allocation of resources to dif- and CL in this rare Polygala. Our objectives were to (i) ferent floral morphs optimizes the use of available energy describe flowering trends and frequencies of all three reserves (Schemske 1978; Schoen and Lloyd 1984). With floral morphs (CH, CL-AG and CL-BG) since they have not resource allocation, production of both floral morphs is been previously described for P. lewtonii, (ii) quantify the independent of each other but one or both are correlated reproductive output of the three floral morphs and (iii) with a resource, typically size (Waller 1980; Steets and explore the selective pressures associated with main- Ashman 2004) or pollinator availability (Culley 2002). taining a mixed-mating strategy. Mixed floral morphs may also be stable by a genetic bal- As previously discussed, there are several hypoth- ance between selfing and cross-pollination. Selfing is eses supporting the maintenance of mixed-mating. 2 AoB PLANTS https://academic.oup.com/aobpla
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